“The role of host demographic storage in the ecological dynamics of heritable symbionts”

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Andrew J. Bibian, Jennifer A. Rudgers, and Tom E. X. Miller

Models inspired by grass-endophyte symbioses show life cycle complexity can alter the dynamics of heritable microbes

The fungal endophyte Epichloë amarillans in seed tissue of the host plant Agrostis hyemalis.
(Credit: Tom E. X. Miller)

Abstract

Heritable symbioses are widespread and ecologically important. Many host organisms have complex life cycles that include diverse opportunities for symbionts to affect their host and be lost during development. Yet, existing theory takes a simplified view of host demography. Here, we generalize symbiosis theory to understand how demographic “storage” in the form of dormant or pre-reproductive life stages can modify symbiosis dynamics. Using grass-endophyte symbioses as context, we developed models to contrast the role of the seed bank (a storage stage) against the reproductive stage in symbiont persistence and prevalence. We find that the seed bank is as or more important than the reproductive stage in driving symbiont dynamics, as long as passage through the seed bank is obligate. Flexible entry to the seed bank substantially weakens its influence on symbiont persistence but can modify prevalence in counter-intuitive ways. Our models identify a role for legacy effects, where hosts that lose symbionts retain their demographic influence. The retention of benefits via legacy effects can reduce symbiont prevalence and even cause prevalence to decline with increasing benefits to hosts because symbiont-free hosts carry those benefits. Our results resolve connections between individual-level host-symbiont interactions and population-level patterns, providing guidance for empirical studies. Read the Article